Diversity and Ecology of Fungi in Mofettes

  • Irena MačekEmail author


Mofettes are extreme environments with ongoing exhalations of ambient temperature geological CO2, which results in relatively constant changes in concentrations of soil gases, in particular CO2 and O2, affecting mofette life. Different aspects in microbial ecology have been studied at several mofette sites, with the majority of the existent studies focusing on soil prokaryotes, while much less work has been done on fungi. Only two groups of fungi have been investigated in mofettes thus far, including arbuscular mycorrhizal fungi, forming arbuscular mycorrhiza, the ubiquitous and ancient symbiosis with plants, and soil and water yeasts. All existent studies clearly show that specific microbial communities form in mofette sites and that they are often abundant in adapted taxa, which can also be described as new to science in some cases (e.g. a new yeast species Occultifur mephitis has been described from the Slovenian mofettes). Therefore, mofette fields can be a rich source of information on how organisms, their populations and communities cope with long-term environmental pressures in their natural habitats. This indicates the potential of mofette systems to serve as natural long-term experimental models in the study of slower ecological and evolutionary processes and in the investigation of the specificity of mofette food webs and ecological networks. In addition, other applications of these systems are being identified, as mofettes serving as models for environmental impact assessments in the case of CO2 leakage from carbon capture and storage (CCS) systems, and research into mofettes being natural reservoirs of potentially hypoxia-tolerant fungal pathogens.


Arbuscular mycorrhizal fungi Elevated CO2 Fungal pathogens Hypoxia Soil biodiversity Yeasts 



This work was supported by the Slovenian Research Agency (ARRS) projects J4-5526, J4-7052 and programme P4-0085. We gratefully acknowledge all of the support given.


  1. Appoloni S, Lekberg Y, Tercek MT, Zabinski CA, Redecker D (2008) Molecular community analysis of arbuscular mycorrhizal fungi in roots of geothermal soils in Yellowstone National Park (USA). Microb Ecol 56:649–659CrossRefGoogle Scholar
  2. Arnold F, West D, Kumar S (1987) Wound healing: the effect of macrophage and tumour derived angiogenesis factors on skin graft vascularization. Br J Exp Pathol 68:569–574PubMedPubMedCentralGoogle Scholar
  3. Beulig F, Heuer VB, Akob DM, Viehweger B, Elvert M, Herrmann M, Hinrichs K-U, Küsel K (2015) Carbon flow from volcanic CO2 into soil microbial communities of a wetland mofette. ISME J 9:746–759CrossRefGoogle Scholar
  4. Beulig F, Urich T, Nowak M, Trumbore SE, Gleixner G, Gilfillan GD, Fjelland KE, Küsel K (2016) Altered carbon turnover processes and microbiomes in soils under long-term extremely high CO2 exposure. Nat Microbiol 1:1–9Google Scholar
  5. Botha A (2006) Yeast in soil. In: Rosa CA, Péter G (eds) The yeast handbook biodiversity and ecophysiology of yeasts. Springer-Verlag, Berlin, pp 221–240CrossRefGoogle Scholar
  6. Botha A (2011) The importance and ecology of yeasts in soil. Soil Biol Biochem 43:1–8CrossRefGoogle Scholar
  7. Brooker RW, Callaway RM (2009) Facilitation in the conceptual melting pot. J Ecol 97:1117–1120CrossRefGoogle Scholar
  8. Cantrell SA, Dianese JC, Fell J, Gunde-Cimerman N, Zalar P (2011) Unusual fungal niches. Mycologia 103:1161–1174CrossRefGoogle Scholar
  9. Collins S, Bell G (2006) Evolution of natural algal populations at elevated CO2. Ecol Lett 9:129–135CrossRefGoogle Scholar
  10. Coyte KZ, Schluter J, Foster KR (2015) The ecology of the microbiome: networks, competition, and stability. Science 350:663–666CrossRefGoogle Scholar
  11. Cramer T, Yamanishi Y, Clausen BE, Förster I, Pawlinski R, Mackman N, Haase VH, Jaenisch R, Corr M, Nizet V, Firestein GS, Gerber HP, Ferrara N, Johnson RS (2003) HIF-1alpha is essential for myeloid cell-mediated inflammation. Cell 112:645–657CrossRefGoogle Scholar
  12. Drake H, Ivarsson M, Bengtson S, Heim C, Siljeström S, Whitehouse MJ, Broman C, Belivanova V, Åström ME (2017) Anaerobic consortia of fungi and sulfate reducing bacteria in deep granite fractures. Nat Commun 8:55CrossRefGoogle Scholar
  13. Dumbrell AJ, Nelson M, Helgason T, Dytham C, Fitter AH (2010) Relative roles of niche and neutral processes in structuring a soil microbial community. ISME J 4:337–345CrossRefGoogle Scholar
  14. Dumbrell AJ, Ashton PD, Aziz N, Feng G, Nelson M, Dytham C, Fitter AH, Helgason T (2011) Distinct seasonal assemblages of arbuscular mycorrhizal fungi revealed by massively parallel pyrosequencing. New Phytol 190:794–804CrossRefGoogle Scholar
  15. Dumbrell AJ, Ferguson RMW, Clark DR (2016) Microbial community analysis by single-amplicon high-throughput next generation sequencing: data analysis – from raw output to ecology. In: McGenity TJ, Timmis KN, Nogales B (eds) Hydrocarbon and lipid microbiology protocols, Springer protocols handbooks. Springer, HeidelbergGoogle Scholar
  16. Erińska M, Silver IA (2001) Tissue oxygen tension and brain sensitivity to hypoxia. Respir Physiol 128:263–276CrossRefGoogle Scholar
  17. Fernández-Montiel I, Pedescoll A, Bécares E (2016) Microbial communities in a range of carbon dioxide fluxes from a natural volcanic vent in Campo de Calatrava, Spain. Int J Greenhouse Gas Control 50:70–79CrossRefGoogle Scholar
  18. Fitter AH (2005) Darkness visible: reflections on underground ecology. J Ecol 93:231–243CrossRefGoogle Scholar
  19. Fitter AH, Moyersoen B (1996) Evolutionary trends in root-microbe symbioses. Philosop Transac Roy Soc B: Biol Sci 351:1367–1375CrossRefGoogle Scholar
  20. Franklin JF (1989) Importance and justification of long-term studies in ecology. In: Likens GE (ed) Long-term studies in ecology: approaches and alternatives. Springer, New York, pp 3–19CrossRefGoogle Scholar
  21. Frerichs J, Oppermann BI, Gwosdz S, Möller I, Herrmann M, Krüger M (2013) Microbial community changes at a terrestrial volcanic CO2 vent induced by soil acidification and anaerobic microhabitats within the soil column. FEMS Microbiol Ecol 84:60–74CrossRefGoogle Scholar
  22. Grahl N, Shepardson KM, Chung D, Cramer RA (2012) Hypoxia and fungal pathogenesis: to air or not to air? Eukaryot Cell 11:560–570CrossRefGoogle Scholar
  23. Gunner HB, Alexander M (1964) Anaerobic growth of Fusarium oxysporum. J Bacteriol 87:1309–1316PubMedPubMedCentralGoogle Scholar
  24. Hall LA, Denning DW (1994) Oxygen requirements of Aspergillus species. J Med Microbiol 41:311–315CrossRefGoogle Scholar
  25. He G, Shankar RA, Chzhan M, Samouilov A, Kuppusamy P, Zweier JL (1999) Noninvasive measurement of anatomic structure and intraluminal oxygenation in the gastrointestinal tract of living mice with spatial and spectral EPR imaging. Proc Natl Acad Sci U S A 96:4586–4591CrossRefGoogle Scholar
  26. Helgason T, Fitter AH (2009) Natural selection and the evolutionary ecology of the arbuscular mycorrhizal fungi (Phylum Glomeromycota). J Exp Bot 60:2465–2480CrossRefGoogle Scholar
  27. Hirabayashi Y, Mahendran R, Koirala S et al (2013) Global flood risk under climate change. Nat Clim Chang 3:816–821CrossRefGoogle Scholar
  28. Hohberg K, Schulz H-J, Balkenhol B, Pilz M, Thomalla A, Russell DJ, Pfanz H (2015) Soil faunal communities from mofette fields: effects of high geogenic carbon dioxide concentration. Soil Biol Biochem 88:420–429CrossRefGoogle Scholar
  29. Hollis JP (1948) Oxygen and carbon dioxide relations of Fusarium oxysporum Schlecht and Fusarium eumartii Carp. Phytopathology 38:761–775Google Scholar
  30. Holloway S, Pearce JM, Hards VL, Ohsumi T, Gale J (2007) Natural emissions of CO2 from the geosphere and their bearing on the geological storage of carbon dioxide. Energy 32:1194–1201CrossRefGoogle Scholar
  31. Karhausen J, Furuta GT, Tomaszewski JE, Johnson RS, Colgan SP, Haase VH (2004) Epithelial hypoxia-inducible factor-1 is protective in murine experimental colitis. J Clin Invest 114:1098–1106CrossRefGoogle Scholar
  32. Kies A, Hengesch O, Tosheva Z, Raschi A, Pfanz H (2015) Diurnal CO2-cycles and temperature regimes in a natural CO2 gas lake. Int J Greenhouse Gas Control 37:142–145CrossRefGoogle Scholar
  33. Krüger M, West J, Frerichs J, Oppermann B, Dictor M-C, Jouliand C, Jones D, Coombs P, Green K, Pearce J, May F, Möller I (2009) Ecosystem effects of elevated CO2 concentrations on microbial populations at a terrestrial CO2 vent at Laacher See, Germany. Energy Procedia 1:1933–1939CrossRefGoogle Scholar
  34. Krüger M, Jones D, Frerichs J, Oppermann BI, West J, Coombs P, Green K, Barlow T, Lister R, Shaw R, Strutt M, Möller I (2011) Effects of elevated CO2 concentrations on the vegetation and microbial populations at a terrestrial CO2 vent at Laacher See, Germany. Int J Greenhouse Gas Control 5:1093–1098CrossRefGoogle Scholar
  35. Kurtzman CP, Fell JW, Boekhoutm T (2011) The yeasts a taxonomic study, 5th edn. Elsevier, AmsterdamGoogle Scholar
  36. Lachance MA (2016) Metschnikowia: half tetrads, a regicide and the fountain of youth. Yeast 33:563–574CrossRefGoogle Scholar
  37. Maček I (2013) A decade of research in mofette areas has given us new insights into adaptation of soil microorganisms to abiotic stress. Acta Agricult Slovenica 101:209–217CrossRefGoogle Scholar
  38. Maček I (2017a) Arbuscular mycorrhizal fungi in hypoxic environments. In: Varma A, Prasad R, Tuteja N (eds) Mycorrhiza – function, diversity, state of the art. Springer, New York, pp 329–348CrossRefGoogle Scholar
  39. Maček I (2017b) Arbuscular mycorrhizal fungal communities pushed over the edge – lessons from extreme ecosystems. In: Lukac M, Grenni P, Gamboni M (eds) Soil biological communities and ecosystem resilience, Book Series: Sustainability in Plant and Crop Protection. Springer, New York, pp 157–172CrossRefGoogle Scholar
  40. Maček I, Pfanz H, Francetič V, Batič F, Vodnik D (2005) Root respiration response to high CO2 concentrations in plants from natural CO2 springs. Environ Exp Bot 54:90–99CrossRefGoogle Scholar
  41. Maček I, Dumbrell AJ, Nelson M, Fitter AH, Vodnik D, Helgason T (2011) Local adaptation to soil hypoxia determines the structure of an arbuscular mycorrhizal fungal community in roots from natural CO2 springs. AEM 77:4770–4777CrossRefGoogle Scholar
  42. Maček I, Kastelec D, Vodnik D (2012) Root colonization with arbuscular mycorrhizal fungi and glomalin-related soil protein (GRSP) concentration in hypoxic soils from natural CO2 springs. Agric Food Sci 21:62–71CrossRefGoogle Scholar
  43. Maček I, Šibanc N, Kavšček M, Lestan D (2016a) Diversity of arbuscular mycorrhizal fungi in metal polluted and EDTA washed garden soils before and after soil revitalization with commercial and indigenous fungal inoculum. Ecol Eng 95:330–339CrossRefGoogle Scholar
  44. Maček I, Vodnik D, Pfanz H, Low-Décarie E, Dumbrell AJ (2016b) Locally extreme environments as natural long-term experiments in ecology. In: Dumbrell AJ, Kordas R, Woodward G, Large scale ecology: model systems to global perspectives. Adv Ecol Res 55:283–323CrossRefGoogle Scholar
  45. Miglietta F, Raschi A, Bettarini I, Resti R, Selvi F (1993) Natural CO2 springs in Italy: a resource for examining long-term response to rising atmospheric CO2 concentrations. Plant Cell Environ 16:873–878CrossRefGoogle Scholar
  46. Nizet V, Johnson RS (2009) Interdependence of hypoxic and innate immune responses. Nat Rev Immunol 9:609–617CrossRefGoogle Scholar
  47. Oppermann BI, Michaelis W, Blumenberg M, Frerichs J, Schulz HM, Schippers A, Beaubien SE, Krüger M (2010) Soil microbial community changes as a result of long-term exposure to a natural CO2 vent. Geochim Cosmochim Acta 74:2697–2716CrossRefGoogle Scholar
  48. Park MK, Myers RA, Marzella L (1992) Oxygen tensions and infections: modulation of microbial growth, activity of antimicrobial agents, and immunologic responses. Clin Infect Dis 14:720–740CrossRefGoogle Scholar
  49. Perata P, Armstrong W, Voesenek LACJ (2011) Plants and flooding stress. New Phytol 190:269–273CrossRefGoogle Scholar
  50. Peyssonaux C, Johnson RS (2004) An unexpected role for hypoxic response: oxygenation and inflammation. Cell Cycle 3:168–171CrossRefGoogle Scholar
  51. Pfanz H, Vodnik D, Wittmann C, Aschan G, Raschi A (2004) Plants and geothermal CO2 exhalations—survival in and adaption to high CO2 environment. Prog Bot 65:499–538CrossRefGoogle Scholar
  52. Rangel DEN, Finlay RD, Hallsworth JE, Dadachova E, Gadd GM (2018) Fungal strategies for dealing with environment- and agriculture-induced stresses. Fungal Biol 122:602–612CrossRefGoogle Scholar
  53. Raschi A, Miglietta F, Tognetti R, van Gardingen P (1997) Plant responses to elevated CO2: evidence from natural springs. Cambridge University Press, Cambridge, p 272CrossRefGoogle Scholar
  54. Schulz H-J, Potapov MB (2010) A new species of Folsomia from mofette fields of the Northwest Czechia (Collembola, Isotomidae). Zootaxa 2553:60–64CrossRefGoogle Scholar
  55. Sharp FR, Bernaudin M (2004) HIF1 and oxygen sensing in the brain. Nat Rev Neurosci 5:437–448CrossRefGoogle Scholar
  56. Šibanc N, Dumbrell AJ, Mandić-Mulec I, Maček I (2014) Impacts of naturally elevated soil CO2 concentrations on communities of soil archaea and bacteria. Soil Biol Biochem 68:348–356CrossRefGoogle Scholar
  57. Šibanc N, Zalar P, Schroers H, Zajc J, Pontes A, Sampaio JP, Maček I (2018) Occultifur mephitis f.a., sp. nov. and other yeast species from hypoxic and elevated CO2 mofette environments. Int J Syst Evol Microbiol 68:2285–2298CrossRefGoogle Scholar
  58. Simmen HP, Battaglia H, Giovanoli P, Blaser J (1994) Analysis of pH, pO2 and pCO2 in drainage fluid allows for rapid detection of infectious complications during the follow-up period after abdominal surgery. Infection 22:386–389CrossRefGoogle Scholar
  59. Simon MC, Keith B (2008) The role of oxygen availability in embryonic development and stem cell function. Nat Rev Mol Cell Biol 4:285–296CrossRefGoogle Scholar
  60. Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press, London, pp 11–145Google Scholar
  61. Tabak HH, Cooke WB (1968) Growth and metabolism of fungi in an atmosphere of nitrogen. Mycologia 60:115–140CrossRefGoogle Scholar
  62. Tylianakis JM, Morris RJ (2017) Ecological networks across environmental gradients. Futuyma DJ (Ed.). Annu Rev Ecol Evol Syst 48:25–48CrossRefGoogle Scholar
  63. Vacher C, Alireza Tamaddoni-Nezhad A, Kamenova S et al (2016) Learning ecological networks from next-generation sequencing data. In: Woodward G, Bohan DA (Eds.) Ecosystem services: from biodiversity to society, PT2. Adv Ecol Res 54:1–39CrossRefGoogle Scholar
  64. van Gardingen PR, Grace J, Harkness DD, Miglietta F, Raschi A (1995) Carbon dioxide emissions at an Italian mineral spring: measurements of average CO2 concentration and air temperature. Agric For Meteorol 73:17–27CrossRefGoogle Scholar
  65. Vodnik D, Kastelec D, Pfanz H, Maček I, Turk B (2006) Small-scale spatial variation in soil CO2 concentration in a natural carbon dioxide spring and some related plant responses. Geoderma 133:309–319CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Biotechnical FacultyUniversity of LjubljanaLjubljanaSlovenia
  2. 2.Faculty of Mathematics, Natural Sciences and Information Technologies (FAMNIT)University of PrimorskaKoperSlovenia

Personalised recommendations